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Phylogeny and Historical Biogeography of Agabinae Diving Beetles (Coleoptera) Inferred from Mitochondrial DNA Sequences

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Phylogeny and Historical Biogeography of Agabinae Diving Beetles (Coleoptera) Inferred from Mitochondrial DNA Sequences MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 30 (2004) 545–562 www.elsevier.com/locate/ympev Phylogeny and historical biogeography of Agabinae diving beetles (Coleoptera) inferred from mitochondrial DNA sequences Ignacio Ribera,a,* Anders N. Nilsson,b and Alfried P. Voglera,c a Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK b Department of Biology and Environmental Science, University of Umea, SE 90187, Umea, Sweden c Department of Biological Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK Received 7 November 2002; revised 27 May 2003 Abstract The Agabinae, with more than 350 species, is one of the most diverse lineages of diving beetles (Dytiscidae). Using the mito- chondrial genes 16S rRNA and cytochrome oxidase I we present a phylogenetic analysis based on 107 species drawn mostly from the four main Holarctic genera. Two of these genera (Ilybius and Ilybiosoma) are consistently recovered as monophyletic with strong support, Platambus is never recovered as monophyletic, and Agabus is found paraphyletic with respect to several of the species groups of Platambus. Basal relationships among the main lineages are poorly defined, although within each of them relationships are in general robust and very consistent across the parameter space, and in agreement with previous morphological analyses. In each of the two most diverse lineages (Ilybius and Agabus including part of Platambus) there is a basal split between Palearctic and Nearctic clades, estimated to have occurred in the late Eocene. The Palearctic clade in turn splits into a Western Palearctic clade and a clade containing mostly Eastern Palearctic species, and assumed to be ancestrally Eastern Palearctic but with numerous transitions to a Holarctic or Nearctic distribution. These results suggest an asymmetry in the colonization routes, as there are very few cases of transcontinental range expansions originating from the Nearctic or the Western Palearctic. According to standard clock estimates, we do not find any transcontinental shift during the Pliocene, but numerous speciation events within each of the continental or subcontinental regions. Ó 2003 Elsevier Inc. All rights reserved. 1. Introduction cludes more than 350 known species in 10 genera, which are mostly distributed in the Holarctic, with only a few Dytiscidae diving beetles, with ca. 3800 known spe- small genera and species groups occurring in South cies (Nilsson, 2001), comprise one of the major lineages America, sub-Saharan Africa, and the Oriental and of aquatic Coleoptera. They are highly modified for Australian regions (Nilsson, 2000, 2001). living in a diversity of continental waters both as larvae The Agabinae is a morphologically homogeneous and adults, showing a wide range of ecological strategies group exhibiting few characters useful for systematics mainly reflected in different swimming behaviors and (Nilsson, 2000). They were traditionally considered a their associated morphotypes (Balke, in press; Ribera tribe within the subfamily Colymbetinae, and placed and Nilsson, 1995). Dytiscids have a world-wide distri- among the basal lineages of Dytiscidae (see, e.g., bution, with the highest species diversity in the tropical Guignot, 1933). Phylogenetic analyses based on 18S and subtropical regions (Balke, in press; Nilsson, 2001). rRNA sequences confirm this basal placement, although However, a few north temperate lineages are very di- the group does not form a monophyletic clade with verse, such as the subfamily Agabinae. The group in- Colymbetini (Ribera et al., 2002a). This is consistent with results obtained by Miller (2001) based on mor- phological characters, who accordingly raised Agabini * Corresponding author. Fax: +44-207-942-5229. to subfamily level. The Agabinae are characterized by E-mail address: [email protected] (I. Ribera). the presence of a linear group of short, stout setae near 1055-7903/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S1055-7903(03)00224-0 546 I. Ribera et al. / Molecular Phylogenetics and Evolution 30 (2004) 545–562 the posterior ventroexternal angle of the metafemur Outgroups included 24 species of all major lineages of (Brinck, 1948; Nilsson, 2000), although some species Dytiscidae with the exception of Hydroporinae and have apparently secondarily lost this character (e.g., Laccophilinae, plus families Hygrobiidae and Amphi- Hydronebrius and some species of Platambus, Nilsson, zoidae (Appendix A). This extensive selection of out- 2000). Attempts to establish natural groups were made groups was considered necessary, as the phylogenetic only recently, but because of the homogeneous mor- position of Agabinae among the basal Dytiscidae lin- phology the delimitation of the Agabinae genera re- eages is still uncertain. All trees were rooted in Amphi- mains problematic (Nilsson, 2000). Two major groups zoidae, which clearly belongs outside Dytiscidae (Miller, of genera can be separated within the subfamily, ac- 2001; Ribera et al., 2002a,b). Rooting the tree in Am- cording to the presence of a ventral setal fringe on the phizoidae allowed the relationships among the remain- female metatibia and the shape of the clypeal fovea: the ing outgroups and the ingroup to vary freely, thus Platynectes group (four genera with a Neotropical and testing the possibly monophyly of Agabinae and the Oriental distribution) and the Agabus group (six genera Agabus group of genera. with mostly Holarctic distribution). Within these gen- Specimens were collected in absolute ethanol, and era, species groups have been defined on the base of muscular tissue used for DNA isolation via a phenol– character combinations, with no robust synapomorphies chloroform extraction as described in Vogler et al. except for some subgenera of Agabus (Nilsson, 2000). (1993) or by extraction columns (Quiagen). Sequences of The Agabinae not only constitute a major element of 16S rRNA (16S) were amplified as a single fragment of the tree of Dytiscidae, they are also of interest to the study ca. 500 bp, using primers 16Sa (50 ATGTTTTTGTT of species richness and historical biogeography. Species AAACAGGCG) and 16Sb (50 CCGGTCTGAACTC differ greatly in the overall size of their geographic ranges, AGATCATGT). A single fragment of ca. 800 bp of COI with some species distributed very widely throughout (from the middle of region E3 to the 30 end, Lund et al., much of the Palearctic, Nearctic, or both. On the other 1996) was amplified using primers ‘‘Jerry’’ (50 CAACA end of the spectrum, some species are limited to narrowly TTTATTTTGATTTTTTGG) and ‘‘Pat’’ (50 TCCAAT defined biogeographic regions, in particular those species GCACTAATCTGCCATATTA) (Simon et al., 1994). It occurring in mountain regions in the southern Palearctic was not possible to obtain PCR products for the COI (e.g., Fery and Nilsson, 1993; Guignot, 1933). fragment of five species (A. affinis, I. bedeli, I. apicalis, In this paper we present mtDNA data for all major P. glabrellus,andA. nannup), and for three species lineages of Agabinae and a large number of the known (A. affinis, A. lapponicus,andP. pictipennis) portions of species, with an emphasis on the Holarctic fauna. We the sequence at the beginning or the end of the sequence also address the main geographical divisions between were missing. For the 16S fragment all specimens were the Palearctic and Nearctic regions, and provide an successfully amplified, except for a small number of base approximate temporal framework for the evolution and pairs at either end of the fragment in some species. All the main vicariance events affecting lineages on both new sequences generated in the study were deposited in sides of the northern Atlantic and Pacific oceans. GenBank under Accession Nos. AY138591–AY138768. Other sequences were obtained from Ribera et al. (2001a,b, 2002b) (Appendix A). 2. Material and methods The following PCR cycling conditions were used for DNA amplification: 10–20 at 95 °C, 3000 at 94 °C, 3000 at 2.1. Taxon sampling and DNA sequencing 47–50 °C (depending on the melting temperatures of the primer pair used), 10–20 at 72 °C (repeated for 35–40 The ingroup included a total of 118 individuals from cycles), and 100 at 72 °C. Amplification products were 107 species in five genera of Agabinae, with representa- purified using a GeneClean II kit (Bio 101). Automated tion of all major lineages (Table 1 and Appendix A). DNA sequencing reagents were supplied by Perkin Sampling was focussed on the larger genera of the Ag- Elmer Applied BioSystems (ABI PRISM Big Dye abus group sensu Nilsson (2000) (Agabus, Ilybius, Plat- Terminator Cycle Sequencing Ready Reaction Kit). ambus, and Ilybiosoma) which has a predominantly Sequencing reactions were purified by ethanol precipi- Holarctic distribution. No specimens of the two smaller tation and were electrophoresed on an ABI3700 se- genera within this group (Hydrotrupes, one species, and quencer. Sequence ambiguities were edited using the Hydronebrius, four species) could be obtained for study. Sequencher 3.0 software package (Gene Codes Due to the taxonomic homogeneity of the genus Ilybio- Corporation). soma, and the difficulty in separating the currently rec- ognized species (Larson et al., 2000), repeated specimens 2.2. Phylogenetic analysis of the only widespread species (I. seriatum) were in- cluded. Voucher specimens are kept in the collections of Sequences for COI were identical in length, and the Natural History Museum (London). there were no major
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